Longitudinal analysis of acute and convalescent B cell responses in a human primary dengue serotype 2 infection model
Acute viral infections induce a rapid and transient increase in antibody-secreting plasmablasts. At convalescence, memory B cells (MBC) and long-lived plasma cells (LLPC) are responsible for long-term humoral immunity. Following an acute viral infection, the specific properties and relationships bet...
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| Published in | EBioMedicine Vol. 41; pp. 465 - 478 |
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| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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Elsevier B.V
01.03.2019
Elsevier |
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| Abstract | Acute viral infections induce a rapid and transient increase in antibody-secreting plasmablasts. At convalescence, memory B cells (MBC) and long-lived plasma cells (LLPC) are responsible for long-term humoral immunity. Following an acute viral infection, the specific properties and relationships between antibodies produced by these B cell compartments are poorly understood.
We utilized a controlled human challenge model of primary dengue virus serotype 2 (DENV2) infection to study acute and convalescent B-cell responses.
The level of DENV2 replication was correlated with the magnitude of the plasmablast response. Functional analysis of plasmablast-derived monoclonal antibodies showed that the DENV2-specific response was dominated by cells producing DENV2 serotype-specific antibodies. DENV2-neutralizing antibodies targeted quaternary structure epitopes centered on domain III of the viral envelope protein (EDIII). Functional analysis of MBC and serum antibodies from the same subjects six months post-challenge revealed maintenance of the serotype-specific response in both compartments. The serum response mainly targeted DENV2 serotype-specific epitopes on EDIII.
Our data suggest overall functional alignment of DENV2-specific responses from the plasmablast, through the MBC and LLPC compartments following primary DENV2 inflection. These results provide enhanced resolution of the temporal and specificity of the B cell compartment in viral infection and serve as framework for evaluation of B cell responses in challenge models.
This study was supported by the Bill and Melinda Gates Foundation and the National Institutes of Health.
•rDEN2Δ30 virus induced plasmablasts two weeks after infection of flavivirus-naïve human subjects.•Expanded plasmablast lineages produced type-specific antibodies including neutralizers to quaternary E protein epitopes•rDEN2Δ30-induced memory B cells retained functional, but not clonal type-specific overlap with the plasmablast response•DENV2-specific antibodies present during convalescence after rDEN2Δ30 infection are highly type-specific.•The rDEN2Δ30 challenge model is a framework against which to evaluate B cell responses to dengue natural infection and vaccination. |
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| AbstractList | Acute viral infections induce a rapid and transient increase in antibody-secreting plasmablasts. At convalescence, memory B cells (MBC) and long-lived plasma cells (LLPC) are responsible for long-term humoral immunity. Following an acute viral infection, the specific properties and relationships between antibodies produced by these B cell compartments are poorly understood.
We utilized a controlled human challenge model of primary dengue virus serotype 2 (DENV2) infection to study acute and convalescent B-cell responses.
The level of DENV2 replication was correlated with the magnitude of the plasmablast response. Functional analysis of plasmablast-derived monoclonal antibodies showed that the DENV2-specific response was dominated by cells producing DENV2 serotype-specific antibodies. DENV2-neutralizing antibodies targeted quaternary structure epitopes centered on domain III of the viral envelope protein (EDIII). Functional analysis of MBC and serum antibodies from the same subjects six months post-challenge revealed maintenance of the serotype-specific response in both compartments. The serum response mainly targeted DENV2 serotype-specific epitopes on EDIII.
Our data suggest overall functional alignment of DENV2-specific responses from the plasmablast, through the MBC and LLPC compartments following primary DENV2 inflection. These results provide enhanced resolution of the temporal and specificity of the B cell compartment in viral infection and serve as framework for evaluation of B cell responses in challenge models.
This study was supported by the Bill and Melinda Gates Foundation and the National Institutes of Health. Acute viral infections induce a rapid and transient increase in antibody-secreting plasmablasts. At convalescence, memory B cells (MBC) and long-lived plasma cells (LLPC) are responsible for long-term humoral immunity. Following an acute viral infection, the specific properties and relationships between antibodies produced by these B cell compartments are poorly understood. We utilized a controlled human challenge model of primary dengue virus serotype 2 (DENV2) infection to study acute and convalescent B-cell responses. The level of DENV2 replication was correlated with the magnitude of the plasmablast response. Functional analysis of plasmablast-derived monoclonal antibodies showed that the DENV2-specific response was dominated by cells producing DENV2 serotype-specific antibodies. DENV2-neutralizing antibodies targeted quaternary structure epitopes centered on domain III of the viral envelope protein (EDIII). Functional analysis of MBC and serum antibodies from the same subjects six months post-challenge revealed maintenance of the serotype-specific response in both compartments. The serum response mainly targeted DENV2 serotype-specific epitopes on EDIII. Our data suggest overall functional alignment of DENV2-specific responses from the plasmablast, through the MBC and LLPC compartments following primary DENV2 inflection. These results provide enhanced resolution of the temporal and specificity of the B cell compartment in viral infection and serve as framework for evaluation of B cell responses in challenge models. This study was supported by the Bill and Melinda Gates Foundation and the National Institutes of Health. •rDEN2Δ30 virus induced plasmablasts two weeks after infection of flavivirus-naïve human subjects.•Expanded plasmablast lineages produced type-specific antibodies including neutralizers to quaternary E protein epitopes•rDEN2Δ30-induced memory B cells retained functional, but not clonal type-specific overlap with the plasmablast response•DENV2-specific antibodies present during convalescence after rDEN2Δ30 infection are highly type-specific.•The rDEN2Δ30 challenge model is a framework against which to evaluate B cell responses to dengue natural infection and vaccination. • rDEN2Δ30 virus induced plasmablasts two weeks after infection of flavivirus-naïve human subjects. • Expanded plasmablast lineages produced type-specific antibodies including neutralizers to quaternary E protein epitopes • rDEN2Δ30-induced memory B cells retained functional, but not clonal type-specific overlap with the plasmablast response • DENV2-specific antibodies present during convalescence after rDEN2Δ30 infection are highly type-specific. • The rDEN2Δ30 challenge model is a framework against which to evaluate B cell responses to dengue natural infection and vaccination. AbstractBackgroundAcute viral infections induce a rapid and transient increase in antibody-secreting plasmablasts. At convalescence, memory B cells (MBC) and long-lived plasma cells (LLPC) are responsible for long-term humoral immunity. Following an acute viral infection, the specific properties and relationships between antibodies produced by these B cell compartments are poorly understood. MethodsWe utilized a controlled human challenge model of primary dengue virus serotype 2 (DENV2) infection to study acute and convalescent B-cell responses. FindingsThe level of DENV2 replication was correlated with the magnitude of the plasmablast response. Functional analysis of plasmablast-derived monoclonal antibodies showed that the DENV2-specific response was dominated by cells producing DENV2 serotype-specific antibodies. DENV2-neutralizing antibodies targeted quaternary structure epitopes centered on domain III of the viral envelope protein (EDIII). Functional analysis of MBC and serum antibodies from the same subjects six months post-challenge revealed maintenance of the serotype-specific response in both compartments. The serum response mainly targeted DENV2 serotype-specific epitopes on EDIII. InterpretationOur data suggest overall functional alignment of DENV2-specific responses from the plasmablast, through the MBC and LLPC compartments following primary DENV2 inflection. These results provide enhanced resolution of the temporal and specificity of the B cell compartment in viral infection and serve as framework for evaluation of B cell responses in challenge models. FundingThis study was supported by the Bill and Melinda Gates Foundation and the National Institutes of Health. Acute viral infections induce a rapid and transient increase in antibody-secreting plasmablasts. At convalescence, memory B cells (MBC) and long-lived plasma cells (LLPC) are responsible for long-term humoral immunity. Following an acute viral infection, the specific properties and relationships between antibodies produced by these B cell compartments are poorly understood.BACKGROUNDAcute viral infections induce a rapid and transient increase in antibody-secreting plasmablasts. At convalescence, memory B cells (MBC) and long-lived plasma cells (LLPC) are responsible for long-term humoral immunity. Following an acute viral infection, the specific properties and relationships between antibodies produced by these B cell compartments are poorly understood.We utilized a controlled human challenge model of primary dengue virus serotype 2 (DENV2) infection to study acute and convalescent B-cell responses.METHODSWe utilized a controlled human challenge model of primary dengue virus serotype 2 (DENV2) infection to study acute and convalescent B-cell responses.The level of DENV2 replication was correlated with the magnitude of the plasmablast response. Functional analysis of plasmablast-derived monoclonal antibodies showed that the DENV2-specific response was dominated by cells producing DENV2 serotype-specific antibodies. DENV2-neutralizing antibodies targeted quaternary structure epitopes centered on domain III of the viral envelope protein (EDIII). Functional analysis of MBC and serum antibodies from the same subjects six months post-challenge revealed maintenance of the serotype-specific response in both compartments. The serum response mainly targeted DENV2 serotype-specific epitopes on EDIII.FINDINGSThe level of DENV2 replication was correlated with the magnitude of the plasmablast response. Functional analysis of plasmablast-derived monoclonal antibodies showed that the DENV2-specific response was dominated by cells producing DENV2 serotype-specific antibodies. DENV2-neutralizing antibodies targeted quaternary structure epitopes centered on domain III of the viral envelope protein (EDIII). Functional analysis of MBC and serum antibodies from the same subjects six months post-challenge revealed maintenance of the serotype-specific response in both compartments. The serum response mainly targeted DENV2 serotype-specific epitopes on EDIII.Our data suggest overall functional alignment of DENV2-specific responses from the plasmablast, through the MBC and LLPC compartments following primary DENV2 inflection. These results provide enhanced resolution of the temporal and specificity of the B cell compartment in viral infection and serve as framework for evaluation of B cell responses in challenge models.INTERPRETATIONOur data suggest overall functional alignment of DENV2-specific responses from the plasmablast, through the MBC and LLPC compartments following primary DENV2 inflection. These results provide enhanced resolution of the temporal and specificity of the B cell compartment in viral infection and serve as framework for evaluation of B cell responses in challenge models.This study was supported by the Bill and Melinda Gates Foundation and the National Institutes of Health.FUNDINGThis study was supported by the Bill and Melinda Gates Foundation and the National Institutes of Health. |
| Author | Pierce, Kristen K. Emerling, Daniel E. Swanstrom, Jesica Diehl, Sean A. Kirkpatrick, Beth D. Durbin, Anna P. Nguyen, Ngan Nivarthi, Usha K. Whitehead, Stephen S. Tu, Huy A. Baric, Ralph S. Delacruz, Matthew J. Patel, Bhumi de Silva, Aravinda M. |
| AuthorAffiliation | f Atreca, Inc. Redwood City, California 94063, USA a Department of Microbiology and Immunology, University of North Carolina School of Medicine, Chapel Hill, North Carolina 27599, USA d Department of International Health, Center for Immunization Research, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD 21205, USA b Department of Microbiology and Molecular Genetics, Vaccine Testing Center, Larner College of Medicine, University of Vermont, Burlington, VT 05405, USA e Laboratory of Infectious Diseases, NIAID, National Institutes of Health, Bethesda, MD 20892, USA c Cellular, Molecular, and Biomedical Sciences Graduate Program, University of Vermont, Burlington, VT 05405, USA |
| AuthorAffiliation_xml | – name: a Department of Microbiology and Immunology, University of North Carolina School of Medicine, Chapel Hill, North Carolina 27599, USA – name: b Department of Microbiology and Molecular Genetics, Vaccine Testing Center, Larner College of Medicine, University of Vermont, Burlington, VT 05405, USA – name: d Department of International Health, Center for Immunization Research, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD 21205, USA – name: f Atreca, Inc. Redwood City, California 94063, USA – name: c Cellular, Molecular, and Biomedical Sciences Graduate Program, University of Vermont, Burlington, VT 05405, USA – name: e Laboratory of Infectious Diseases, NIAID, National Institutes of Health, Bethesda, MD 20892, USA |
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| Keywords | Antibody Viral infection Dengue Humoral immunity |
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| Snippet | Acute viral infections induce a rapid and transient increase in antibody-secreting plasmablasts. At convalescence, memory B cells (MBC) and long-lived plasma... AbstractBackgroundAcute viral infections induce a rapid and transient increase in antibody-secreting plasmablasts. At convalescence, memory B cells (MBC) and... • rDEN2Δ30 virus induced plasmablasts two weeks after infection of flavivirus-naïve human subjects. • Expanded plasmablast lineages produced type-specific... |
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| SubjectTerms | Acute Disease Advanced Basic Science Antibodies, Neutralizing - blood Antibodies, Neutralizing - immunology Antibody B-Lymphocytes - cytology B-Lymphocytes - immunology B-Lymphocytes - metabolism Dengue Dengue - diagnosis Dengue - virology Dengue Virus - genetics Dengue Virus - isolation & purification Epitope Mapping Epitopes - immunology Humans Humoral immunity Internal Medicine Leukocytes, Mononuclear - cytology Leukocytes, Mononuclear - virology Longitudinal Studies Plasma Cells - cytology Plasma Cells - metabolism Research paper Serogroup Viral Envelope Proteins - immunology Viral infection |
| Title | Longitudinal analysis of acute and convalescent B cell responses in a human primary dengue serotype 2 infection model |
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